Maturation and functional integration of new granule cells into the adult hippocampus

Cold Spring Harbor Perspectives in Biology

Volumn 8, Issue 1, 2016, Pages

  Toni, Nicolas ^a   Schinder, Alejandro F ^b  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MODEL; CYTOLOGY; DENTATE GYRUS; GROWTH, DEVELOPMENT AND AGING; HIPPOCAMPUS; NERVE CELL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; SYNAPSE;

DENTATE GYRUS; HIPPOCAMPUS; MODELS, BIOLOGICAL; NERVE NET; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; SYNAPSES;

EID: 84953295438     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a018903     Document Type: Review

References (83)

1. Acsady L, Kamondi A, Sik A, Freund T, Buzsaki G. 1998. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18: 3386-3403.
2. Amaral DG. 1978. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182: 851-914.
3. Amaral DG, Ishizuka N, Claiborne B. 1990. Neurons, numbers and the hippocampal network. Prog Brain Res 83: 1-11.
4. Amaral DG, Scharfman HE, Lavenex P. 2007. The dentate gyrus: Fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163: 3-22.
5. Barria A, Malinow R. 2005. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 48: 289-301.
6. Beckervordersandforth R, Zhang C-L, Lie DC. 2015. Transcription factor-dependent control of adult hippocampal neurogenesis. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a018879.
7. Ben Ari Y. 2002. Excitatory actions of GABA during development: The nature of the nurture. Nat Rev Neurosci 3: 728-739.
8. Bergami M, Masserdotti G, Temprana SG, Motori E, Eriksson TM, Gobel J, Yang SM, Conzelmann KK, Schinder AF, Götz M, et al. 2015. A critical period for experiencedependent remodeling of adult-born neuron connectivity. Neuron 85: 710-717.
9. Blaesse P, Airaksinen MS, Rivera C, Kaila K. 2009. Cationchloride cotransporters and neuronal function. Neuron 61: 820-838.
10. Bonaguidi MA,Wheeler MA, Shapiro JS, Stadel RP, Sun GJ, Ming GL, Song H. 2011. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145: 1142-1155.
11. Bonaguidi MA, Song J, Ming GL, Song H. 2012. A unifying hypothesis on mammalian neural stem cell properties in the adult hippocampus. Curr Opin Neurobiol 22: 765- 761.
12. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268.
13. Buckmaster PS, Strowbridge BW, Kunkel DD, Schmiege DL, Schwartzkroin PA. 1992.Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus 2: 349-362.
14. Buffelli M, Burgess RW, Feng G, Lobe CG, Lichtman JW, Sanes JR. 2003. Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424: 430-434.
15. Chancey JH, Adlaf EW, Sapp MC, Pugh PC, Wadiche JI, Overstreet-Wadiche LS. 2013. GABA depolarization is required for experience-dependent synapse unsilencing in adult-born neurons. J Neurosci 33: 6614-6622.
16. Choe Y, Pleasure SJ, Mira H. 2015. Control of adult neurogenesis by short-range morphogenic signaling molecules. Cold Spring Harb Perspect Biol doi: 10.1101/cshper spect.a018887.
17. Claiborne BJ, Amaral DG, Cowan WM. 1990. Quantitative, three-dimensional analysis of granule cell dendrites in the rat dentate gyrus. J Comp Neurol 302: 206-219.
18. Couillard-Despres S, Winner B, Karl C, Lindemann G, Schmid P, Aigner R, Laemke J, Bogdahn U, Winkler J, Bischofberger J, et al. 2006. Targeted transgene expression in neuronal precursors: Watching young neurons in the old brain. Eur J Neurosci 24: 1535-1545.
19. Deshpande A, Bergami M, Ghanem A, Conzelmann KK, Lepier A, Götz M, Berninger B. 2013. Retrograde monosynaptic tracing reveals the temporal evolution of inputs onto new neurons in the adult dentate gyrus and olfactory bulb. Proc Natl Acad Sci 110: E1152-E1161.
20. DesmondNL, Levy WB. 1985. Granule cell dendritic spine density in the rat hippocampus varies with spine shape and location. Neurosci Lett 54: 219-224.
21. Espó sito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF. 2005. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25: 10074-10086.
22. Faulkner RL, Jang MH, Liu XB, Duan X, Sailor KA, Kim JY, Ge S, Jones EG, Ming GL, Song H, et al. 2008. Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain. Proc Natl Acad Sci 105: 14157-14162.
23. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6: 347-470.
24. Frotscher M, Seress L, Schwerdtfeger WK, Buhl E. 1991. The mossy cells of the fascia dentata: A comparative study of their fine structure and synaptic connections in rodents and primates. J Comp Neurol 312: 145-163.
25. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439: 589-593.
26. Ge S, Yang CH, Hsu KS, Ming GL, Song H. 2007. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54: 559-566.
27. Ge S, Sailor KA, Ming GL, Song H. 2008. Synaptic integration and plasticity of new neurons in the adult hippocampus. J Physiol 586: 3759-3765.
28. Götz M, Nakafuku M, Petrik D. 2015. Neurogenesis in the developing adult brain-Similarities and key differences. Cold Spring Harb Perspect Biol doi: 10.1101/cshper spect.a018853.
29. Gu Y, Arruda-Carvalho M, Wang J, Janoschka SR, Josselyn SA, FranklandPW, Ge S. 2012. Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 15: 1700-1706.
30. Han ZS, Buhl EH, Lorinczi Z, Somogyi P. 1993. A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5: 395-410.
31. Henze DA, Wittner L, Buzsaki G. 2002. Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci 5: 790-795.
32. Hosp JA, Struber M, Yanagawa Y, Obata K, Vida I, Jonas P, Bartos M. 2013. Morpho-physiological criteria divide dentate gyrus interneurons into classes. Hippocampus 24: 189-203.
33. Houser CR. 2007. Interneurons of the dentate gyrus: An overview of cell types, terminal fields and neurochemical identity. Prog Brain Res 163: 217-232.
34. Jones SP, Rahimi O, O'Boyle MP, Diaz DL, Claiborne BJ. 2003. Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3. Hippocampus 13: 413-427.
35. Karten YJ, Jones MA, Jeurling SI, Cameron HA. 2006. GABAergic signaling in young granule cells in the adult rat and mouse dentate gyrus. Hippocampus 16: 312-320.
36. Kempermann G. 2015.Activity dependency and aging in the regulation of adult neurogenesis. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a018929.
37. KempermannG, Gast D, Kronenberg G, Yamaguchi M, Gage FH. 2003. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130: 391-399.
38. Kronenberg G, Reuter K, Steiner B, BrandtMD, Jessberger S, Yamaguchi M, Kempermann G. 2003. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J CompNeurol 467: 455-463.
39. Kuhn HG. 2015. Control of cell survival in adult neurogenesis. Cold Spring Harb Perspect Biol doi: 10.1101/cshper spect.a018895.
40. Kunze A, Congreso MR, Hartmann C, Wallraff-Beck A, Huttmann K, Bedner P, Requardt R, Seifert G, Redecker C,Willecke K, et al. 2009. Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci 106: 11336-11341.
41. Lacefield CO, Itskov V, Reardon T, Hen R, Gordon JA. 2010. Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus. Hippocampus 22: 106-116.
42. Laplagne DA, Espó sito MS, Piatti VC, Morgenstern NA, Zhao C, van Praag H, Gage FH, Schinder AF. 2006. Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 4: e409.
43. LaplagneDA, Kamienkowski JE, Espó sito MS, Piatti VC, Zhao C, Gage FH, Schinder AF. 2007. Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur J Neurosci 25: 2973-2981.
44. Li X, Gutierrez DV, Hanson MG, Han J, MarkMD, Chiel H, Hegemann P, Landmesser LT, Herlitze S. 2005. Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc Natl Acad Sci 102: 17816-17821.
45. Li Y, Aimone JB, Xu X, Callaway EM, Gage FH. 2012. Development of GABAergic inputs controls the contribution of maturing neurons to the adult hippocampal network. Proc Natl Acad Sci 109: 4290-4295.
46. Li Y, Stam FJ, Aimone JB, Goulding M, Callaway EM, Gage FH. 2013.Molecular layer perforant path-associated cells contribute to feed-forward inhibition in the adult dentate gyrus. Proc Natl Acad Sci 110: 9106-9111.
47. Lucassen PJ, Oomen CA, Naninck EFG, Fitzsimons CP, van Dam AM, Czeh B, Korosi A. 2015. Regulation of adult neurogenesis and plasticity by (early) stress, glucocorticoids, and inflammation. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a021303.
48. Marin-Burgin A,Mongiat LA, Pardi MB, Schinder AF. 2012. Unique processing during a period of high excitation/ inhibition balance in adult-born neurons. Science 335: 1238-1242.
49. Markwardt SJ, Dieni CV,Wadiche JI, Overstreet-Wadiche L. 2011. Ivy/neurogliaform interneurons coordinate activity in the neurogenic niche. Nat Neurosci 14: 1407-1409.
50. Massa F, Koehl M,Wiesner T, Grosjean N, Revest JM, Piazza PV, Abrous DN, Oliet SH. 2011.Conditional reduction of adult neurogenesis impairs bidirectional hippocampal synaptic plasticity. Proc Natl Acad Sci 108: 6644-6649.
51. Mathews EA, Morgenstern NA, Piatti VC, Zhao C, Jessberger S, Schinder AF, Gage FH. 2010. A distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesis. J Comp Neurol 518: 4479-4490.
52. McBain CJ. 2008. Differential mechanisms of transmission and plasticity at mossy fiber synapses. Prog Brain Res 169: 225-240.
53. Mongiat LA, Espó sito MS, Lombardi G, Schinder AF. 2009. Reliable activation of immature neurons in the adult hippocampus. PLoS ONE 4: e5320.
54. MuY, Zhao C, Gage FH. 2011. Dopaminergic modulation of cortical inputs during maturation of adult-born dentate granule cells. J Neurosci 31: 4113-4123.
55. Neunuebel JP, Knierim JJ. 2012. Spatial firing correlates of physiologically distinct cell types of the rat dentate gyrus. J Neurosci 32: 3848-3858.
56. Neves G, Cooke SF, Bliss TV. 2008. Synaptic plasticity, memory and the hippocampus: A neural network approach to causality. Nat Rev Neurosci 9: 65-75.
57. Overstreet-Wadiche LS, Bromberg DA, Bensen AL, Westbrook GL. 2005. GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94: 4528-4532.
58. Overstreet-Wadiche LS, Bensen AL, Westbrook GL. 2006a. Delayed development of adult-generated granule cells in dentate gyrus. J Neurosci 26: 2326-2334.
59. Overstreet-Wadiche LS, Bromberg DA, Bensen AL, Westbrook GL. 2006b. Seizures accelerate functional integration of adult-generated granule cells. J Neurosci 26: 4095-4103.
60. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. 1997. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17: 3727-3738.
61. Piatti VC, Davies-Sala MG, Esposito MS,Mongiat LA, Trinchero MF, Schinder AF. 2011. The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci 31: 7715-7728.
62. Schmidt-Hieber C, Jonas P, Bischofberger J. 2004. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429: 184-187.
63. Snyder JS, Kee N,Wojtowicz JM. 2001. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 85: 2423-2431.
64. Song J, Zhong C, Bonaguidi MA, Sun GJ, Hsu D, Gu Y, Meletis K, Huang ZJ, Ge S, Enikolopov G, et al. 2012. Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 489: 150-154.
65. Song J, Olsen RHJ, Sun J, Ming G-L, Song H. 2015.Neuronal circuitry mechanisms regulating adult mammalian neurogenesis. Cold Spring Harb Perspect Biol doi: 10.1101/ cshperspect.a018937.
66. 2β signalling in young and mature hippocampal granule cells. J Physiol 586: 3795-3811.
67. Sun GJ, Sailor KA,MahmoodQA, Chavali N, Christian KM, Song H, Ming GL. 2013. Seamless reconstruction of intact adult-born neurons by serial end-block imaging reveals complex axonal guidance and development in the adult hippocampus. J Neurosci 33: 11400-11411.
68. Tashiro A, Zhao C, Gage FH. 2006. Retrovirus-mediated single-cell gene knockout technique in adult newborn neurons in vivo. Nat Protoc 1: 3049-3055.
69. Temprana SG,Mongiat LA, Yang SM, Trinchero MF, Alvarez DD, Kropff E, Giacomini D, Beltramone N, Lanuza GM, Schinder AF. 2015. Delayed coupling to feedback inhibition during a critical period for the integration of adultborn granule cells. Neuron 85: 116-130.
70. Toni N, Sultan S. 2011. Synapse formation on adult-born hippocampal neurons. Eur J Neurosci 33: 1062-1068.
71. Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH. 2007. Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10: 727-734.
72. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF. 2008.Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11: 901-907.
73. Torborg CL, Nakashiba T, Tonegawa S, McBain CJ. 2010. Control of CA3 output by feedforward inhibition despite developmental changes in the excitation-inhibition balance. J Neurosci 30: 15628-15637.
74. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T. 2005. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47: 803- 815.
75. Tronel S, Fabre A, Charrier V, Oliet SH, Gage FH, Abrous DN. 2010. Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc Natl Acad Sci 107: 7963-7968.
76. van Praag H, Kempermann G, Gage FH. 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2: 266-270.
77. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
78. van Strien NM, Cappaert NL, Witter MP. 2009. The anatomy of memory: An interactive overview of the parahippocampal- hippocampal network. Nat Rev Neurosci 10: 272-282.
79. Vivar C, Potter MC, Choi J, Lee JY, Stringer TP, Callaway EM, Gage FH, Suh H, van Praag H. 2012. Monosynaptic inputs to new neurons in the dentate gyrus.Nat Commun 3: 1107.
80. WangS, Scott BW,Wojtowicz JM. 2000. Heterogenous properties of dentate granule neurons in the adult rat. JNeurobiol 42: 248-257.
81. Wang LP, Kempermann G, Kettenmann H. 2005. A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 29: 181-189.
82. Wickersham IR, Lyon DC, Barnard RJ, Mori T, Finke S, Conzelmann KK, Young JA, Callaway EM. 2007. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53: 639-647.
83. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH. 2006. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26: 3-11.